From the Canary Islands

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From the Canary Islands JOURNAL OF CON C HOLOG Y (2010), VOL .40, NO.2 143 ACTIVE DISGUISE IN LAND SNAILS: NAPAEUS BADIOSUS (GASTROPODA, PULMONATA, ENIDAE) FROM THE CANARY ISLANDS 1 2 3 4 4,5 YURENA YANES , JAVIER MARTÍN , JUAN D. DELGA D O , MARÍA R. ALONSO & MIGUEL IBÁÑEZ 1Roy M. Huffington Department of Earth Sciences, Southern Methodist University, Dallas, TX 75275–0395, USA 2El Coromoto, La Laguna, Tenerife, Canary Islands, Spain 3Área de Ecología, Dept. Sistemas Físicos, Químicos y Naturales, Univ. Pablo de Olavide, Ctra. de Utrera, km 1, 41013 Sevilla, Spain 4Department of Animal Biology, La Laguna University, E–38206 La Laguna, Tenerife, Canary Islands, Spain Abstract Some snails disguise the shell with a covering of soil or other material. Among species in the Canarian enid genus Napaeus, some rock-dwelling species cover the shell with lichens; in one of these, N. barquini, the process is known to be active. In some ground-dwelling species the muddy covering may be acquired passively, as for example in N. variatus. Napaeus badiosus is a snail with an almost smooth shell which is not disguised in the field. It normally rests out of sight of predators. Four specimens of N. badiosus were transferred to a glass terrarium with a layer of loose, humid soil without stones and vegetation. The snails acquired a soil layer with prominent protuberances that covered the whole shell, reducing the risk of attack by visual predators. The appearance of the disguised N. badiosus shell is compared with those of N. barquini and of N. variatus. The disguise of N. badiosus is similar to that of N. barquini. This active disguise thus appears to be facultative, adopted when hiding places are not available. Mechanisms of disguise are briefly discussed; the behaviour of other disguised species should be investigated. Key words active disguise, predation, land snail, Napaeus, Canary Islands INTRODUCT I ON process by which this layer is positioned on the shell remains unknown. It may be acquired pas- The fitness of many organisms depends on mini- sively by passage through a sticky substrate, or mising the risk of predation (Palma and Steneck, by adherence to ribs, hairs or spines on the shell, 2001; Ruxton et al., 2004). In land snails, an as in the Canarian hygromiid Monilearia tubae- important anti-predator adaptation is the cryptic formis Alonso & Groh 2006, which inhabits dry colouration of the shell and/or body colouration areas of Fuerteventura Island. This species has (Allen, 2004), which decreases the chances of the a shell with sharp, densely-packed ribs (Ibáñez animal being seen against its background. This et al., 2006) and is covered with an additional thin crypsis is usually achieved through the coloura- and relatively uniform layer of soil. tion of the organism itself. However, some ani- Among Canarian enids, there are many species mals increase their crypsis by actively decorating which acquire this external covering. Passive themselves with inanimate or animate compo- disguise seems likely in the case of Napaeus var- nents of their habitat. This strategy is well known iatus (Webb & Berthelot 1833), which lives in the among insects and marine crustaceans and mol- northern coastal zone of Tenerife (Fig. 1). These luscs but is unusual among land snails and slugs, snails are ground dwellers and usually have the perhaps because these are typically nocturnal shell (height: 11–15 mm) covered with a relatively and thus less liable to attack by visually-hunting uniform, almost tubular, layer of wet soil (Alonso predators (Runham & Hunter, 1970). In some et al., 1995; Fig. 2 A), which can easily stick to land snail species, however, the shell often has their shells; the disguise probably is acquired an additional external layer, usually consisting during the snail movement in the muddy soil. of dust or soil. There are an increasing number of Similar disguised appearances have been found studies showing such external disguise in snails, in N. tenoensis Henríquez 1993 (Henríquez et al., especially enids, in natural settings (Fechter 1993) and N. helvolus (Webb & Berthelot 1833) & Falkner, 1990; Falkner, 1992; Gittenberger & (personal observation, 2008), two species also Menkhorst, 1993; Gittenberger, 1996; Herbert and from the northern coastal zone of Tenerife. Kilburn, 2004; Allgaier, 2007). In many cases the However, the case of six rock-dwelling Napaeus species endemic to the Canary Islands is dif- Contact author : [email protected] ferent. All six have glossy, weakly ornamented 144 Y YANES , J MARTÍN , JD DELGA D O , MR ALONSO & M IBÁÑEZ Figure 1 Geographic distribution of Napaeus variatus and N. badiosus; symbols represent 1 × 1 km UTM squares. and smooth shells, with no hairs, and a similar, of these Napaeus species have relatively smooth small size (shell height: 8–13 mm): N. gruereanus shells, passive disguise with lichens of the rock (Grasset 1857), from El Hierro, N. barquini Alonso faces seems unlikely. In one case, Napaeus barquini, & Ibáñez 2006, and N. beguirae Henríquez 1995, the active process of acquiring disguise has been from La Gomera, N. roccellicola (Webb & Berthelot observed. It grazes lichen and/or soil material 1833), from Tenerife, N. lichenicola Alonso & from the substrate and sticks it to the surface Ibáñez 2007, from Fuerteventura and N. rufobrun- of its shell with the mouth, forming protuber- neus (Wollaston 1878), from Lanzarote. By day, all ances and altering the appearance of the shell these species usually rest in a quiescent state on considerably (Allgaier, 2007: a visual demonstra- open, lichen-covered rock faces exposed to the tion of the process is available at http://home. humid trade winds. All six species normally have arcor.de/christoph.allgaier/videofile.htm). It is shells disguised by an additional layer made most probable that the other species also pursue from surrounding lichens, including Roccella sp. an “active disguise” strategy. Two species, N. (the orchill, a fruticose lichen) in N. roccellicola, gruereanus and N. roccellicola, have been found and crustose lichens in all other five Napaeus without disguise in other habitats such as the hol- species (Wollaston, 1878; Alonso et al., 1995, 2006; lows of stone walls and Euphorbia sp. scrublands, Allgaier, 2007; Ibáñez et al., 2007). Since all six respectively. AC TIVE D ISGUISE IN LAN D SNAILS 145 small shell weakly ornamented and relatively smooth (Figs 2 B, C). MATER I AL EXA mi NED N. badiosus (shell height: 12–13 mm), occurs between 15–550 m altitude in a dry, lowland vegetation area of the southern slopes of central and eastern Tenerife mountains (Fig. 1). The snails are mostly active at night or during wet weather, resting the remaining time under stones or in rock crevices, with the shell aperture tightly adhered to a stone or a rock crevice wall via an epiphragm of dried mucus. In contrast to the other six active-disguised Napaeus species above mentioned, N. badiosus did not show disguise at any locality (Fig. 1). This is not surprising given that the species usually lives in an arid environment which would presumably makes passive disguise more difficult, and where there are plenty of hiding places. Four living, undisguised N. badiosus specimens were captured in a rock crevice at Mirador de San Martín (Güímar, leeward slope of Tenerife Island). They were transferred in the laboratory to a glass terrarium (20×12×10 cm) layered with a loose, moist, standard greenhouse soil, free of stones and vegetation. RESULTS AND DI SCUESS I ON Each N. badiosus specimen actively used the soil to cover the surface of their shell during the night of their transfer to the terrarium, work- Figure 2 A, Napaeus variatus from Los Realejos, north of Tenerife Island. The specimen was placed on a stone ing from the apex to the aperture. Later, they to easier visualization. B, a N. variatus specimen with all adhered to the terrarium walls by means the shell cleaned. C, Napaeus badiosus from Mirador de of an epiphragm of dried mucus (Figs 3 A, San Martín (Güímar, south of Tenerife Island). B). The shell-cover was incomplete; a tiny area of about 3 mm2 remained soil-free at the base of the body whorl close to the shell aperture Disguised snails are easily overlooked in the (Figs 3 A, B, arrow and asterisks), making easier field. However, the nine disguised species above a tight seal between the shell aperture and the mentioned represent the 16% of the 56 known underlying surface through the epiphragm. A Napaeus species (Yanes et al., 2009) and it is pos- similar uncovered shell area in N. barquini was sible that other Napaeus species can also disguise. named “gap area” by Allgaier (2007). The four Here we report a new case of active disguise specimens had an extraneous layer arranged in with soil material in a tenth Napaeus species, N. the form of prominent soil protuberances alter- badiosus (Webb and Berthelot 1833), contrasted ing greatly the appearance of the shell, making with the possibly passive disguise of N. variatus it virtually unrecognisable to the human eye (Webb & Berthelot 1833). Both species have a (Fig. 3 D), and therefore presumably reducing 146 Y YANES , J MARTÍN , JD DELGA D O , MR ALONSO & M IBÁÑEZ Figure 3 A–C, Three views of the disguised shell of Napaeus badiosus. A, lateral view. B, almost ventral view. C, dorsal view. The dashed line in “A” represents the joining plane, parallel to the snail shell aperture and nearly perpendicular to the photograph plane. The arrow and asterisks in “A” and “B” represent the uncovered “gap area”. D, View of the terrarium base, with three disguised specimens of Napaeus badiosus on the humid soil; the fourth specimen, with a cleaned shell, was added for comparison. AC TIVE D ISGUISE IN LAN D SNAILS 147 the risk of visual predation.
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